Dragon Quest VIII uses cel-shading textures for the characters and scenery and is the first game in the series to have fully three dimensional environments. This game retains most of the series' role-playing game elements, such as turn-based combat and the experience level system. Dragon Quest VIII follows the silent Hero, the main character, and his party of allies as they journey towards their goal of defeating the wicked Dhoulmagus. The kingdom of Trodain has been cursed by Dhoulmagus and the King, Trode, and his daughter, Medea, have both been transformed and it is up to the Hero to return them to their original form and save the kingdom.

In Dragon Quest VIII, the player controls the Hero in a fully three-dimensional environment, utilizing the left analog stick or D-pad on the PlayStation controller to move him. Using the right analog stick, players can pan the camera a full 360 degrees around the character or in a first-person perspective. The visual controls allow players to examine people and objects more closely than the top-down perspective of the game's predecessors. With a new fully-integrated world, towns and dungeons are no longer identified by two-dimensional icons found on the world maps. Players can guide the Hero across vast landscapes to reach full-size towns and buildings.